3. The validity of the concept of an international growth reference

There are problems associated with the use of any growth reference
internationally. Currently, the NCHS growth references are promoted for
international use, and the final part of this article is a critique of such use.
In nutritional assessment, growth references may be used either
cross-sectionally, or longitudinally. If used cross-sectionally, there are
problems with the choice of cut-off. The NCHS centiles are smoothed, using cubic
spline curves (National Center for Health Statistics, 1977). This modelling
procedure concentrates on the goodness of fit and smoothness of individual
centiles, but pays no attention to the spacing between centiles, making no
allowance for skewness in the data (Cole, 1989). Thus the highest and lowest
centiles (95th and 5th, respectively) are often incorrect, and the potential for
misclassification if the 5th centile is used as a cutoff may be large. It is
perhaps more appropriate to use Z scores as cut-offs for screening. This is
another statistical construct, but one which allows a variety of cut-offs to be
chosen, including ones which are well below the 5th centile, but which may be
useful in nutritional classification of populations in which stunting is both
widespread and severe. However, there are problems associated with the use of Z
scores. In particular, there is the possibility of misclassification, even of
sections of well-off populations. Table 2 shows the proportion of 7-year-old
males from various populations in industrialized nations, and populations of
high socio-economic status in developing countries which fall below -2 Z scores
of the NCHS references for height for age.

If the NCHS references give a perfect fit for other populations
which achieve, or are close to achieving their genetic potential for growth,
then it would be expected that 2.3% of each population would fall below -2 Z
scores of NCHS. For the Northern European populations of Netherlands, Sweden and
Britain (London), the proportions falling below -2 Z scores are considerably
lower than 2.3%. For the Canadian population the proportion falling below -2 Z
scores is close to this value, while for the Southern European populations of
Spain and Italy the proportions are 3.1 and 4.1% respectively. Although it is
not clear if the secular trend has stopped in these two countries, the overall
picture supports the view that North American growth patterns are a hybrid of
Northern and Southern European growth patterns.

For high socio-economic status African, and African origin
populations in industrialized nations, the proportions falling below -2 Z scores
of NCHS are considerably lower for four of the groups examined, similar for one
of them, and higher in two of them. For Indo-Mediterranean populations, the
extent of misclassification of normals is lower than for European populations,
while for the Asiatic groups examined, the proportion of children falling below
-2 Z scores of NCHS is close to the expected 2.3% for four of them, slightly
lower for one, and much higher in two of them. Therefore, if there is the
possibility of misclassifying a proportion of any group which is believed to
have similar genetic potential for growth, there is also the possibility of
misclassification of less well off groups, for the same reason.

Longitudinal use of the NCHS growth references is also
problematic. The most important problem is that the now traditional assumption
that under good environmental conditions children track along a particular
centile is not strictly correct. Although it is often assumed that
pre-adolescent growth in length, and subsequently height, is a smooth and
continuous process, a number of studies have shown that the growth patterns of
individual children are more likely to be cyclical, with measured height
oscillating about a centile line, rather than tracking it. Indeed, the normal
growth curve, although representing population growth phenomena quite well, is
not such a good representation of any individual growth pattern. Growth
phenomena observed to contradict the tracking principle include: (1) catch-up
and catch-down growth in the first two years of life (Smith et al.,
1976); (2) mini growth spurts (Hermanussen, 1988); (3) seasonality of growth
(Cole, 1993); and (4) biennial cyclicity of growth, shown to take place in
children between the ages of 3 and 11 years (Butler, McKie & Ratcliffe,
1989).

Catch-up and catch-down growth usually take place in the first two
years of life. During this time, children may cross the centile lines either
upwards or downwards, rather than tracking along them. Catch-up growth can occur
after a period of restricted growth in utero. The mini growth spurt was first
described for healthy German children, whose knee height was measured on a daily
basis (Hermanussen et al., 1988). These spurts occur with a cyclicity of
between 30 and 55 days. Hermanussen et al. (1988) give examples of
individuals showing this phenomenon, and it appears that there is a 3-4 fold
variation in the rate of skeletal growth between the fastest and slowest time of
growth. For a girl aged 6.6 years, the maximum growth rate of the lower leg was
3.6 cm/year, the minimum 1.1 cm/year. For a boy aged 8.9 years, the maximum and
minimum rates were 4.2 and 1.1 cm/year, respectively. Another type of deviation
from the tracking principle is the seasonality of growth reported for children
in Japan (Togo & Togo, 1982), the Orkneys (Marshall, 1975) and Cambridge
(Cole, 1993). The broad consensus is that height velocity is greatest in the
spring, weight velocity is greatest in the fall (Cole, 1993).

Table 2. Proportion of males aged 7 years below -2 Z scores
of National Center for Health Statistics (1977) references of height for age,
for various populations in industrialised nations, or of high socio-economic
status in developing countries

Population

% < -2 Z scores

Reference

European and European origin

Netherlands

0.2

Roede & van Wieringen, 1985

Sweden

0.4

Lindgren & Strandell, 1986

Norway

0.5

Waaler, 1984

UK (London)

0.9

Cameron, 1979

Canada

2.7

Shephard et al., 1984

Spain

3.1

Hernandez et al., 1985

Italy

4.1

Kramer, 1983

African and African origin

Jamaica, high socio-economic status

0.1

Ashcroft & Lovell, 1964

Nigeria, high socio-economic status

0.3

Janes, unpublished, in Eveleth & Tanner, 1990

African British

0.4

Ulijaszek, 1987

African American (NHANES I & II)

0.9

Frisancho, 1990

Haiti

2.9

King et al., 1963

African American (NCHS)

4.7

unpublished, in Eveleth & Tanner, 1990

Turkana

10.7

Little et al., 1983

Indo-Mediterranean

India, high socio-economic status (Chandigarh)

0.5

Prakash & Cameron, 1981

Turkish, in Sweden

0.7

Mjönes, 1987

Pakistani, Britain

0.7

Peters & Ulijaszek, unpublished data

East African Asians, Britain

1.6

Peters & Ulijaszek, unpublished data

Sikhs, Britain

1.8

Peters & Ulijaszek, unpublished data

Indian Hindus, Britain

4.2

Peters & Ulijaszek, unpublished data

Asiatic

Koreans in Japan

0.9

Kim, 1982

Japanese

1.4

Kikuta & Takaishi, 1987

Japanese, Kyoto

1.8

Tanner et al., 1982

Japan, national sample

2.0

Tanner et al., 1982

China, urban

2.9

Zhang & Huang, 1988

Chinese in Jamaica

5.4

Ashcroft & Lovell, 1964

Southern Chinese, Hong Kong

6.7

Chang et al., 1963

Another phenomenon which is at odds with the tracking principle is
that of mid-childhood cyclicity of growth. A study in Edinburgh of mid-childhood
growth of 80 boys and 55 girls between the ages of 3 and 11 years showed a
cyclicity of statural growth with a periodicity of 2.2 years in males, 2.1 years
in females (Butler et al., 1989). Although cyclicity of growth was
observed in all the children, periodicity and magnitude of peak growth rates
varied.

If, in any individual, there are several cyclicities of growth
operating, then it is difficult to interpret growth patterns on the basis of a
small number of measurements across time. There is a need to identify deviation
from the growth references as early as possible. However, under some
circumstances growth cyclicity may indicate such deviation in an individual for
reasons other than growth faltering.

Any use of growth references internationally should acknowledge
that they can act, at best, as imperfect yardsticks, since human populations may
show similar growth characteristics, but are unlikely ever to become so
homogeneous that they show the same genetic potential for growth. Since the NCHS
growth references do not represent the greatest possible human potential for
growth, they may not be any more appropriate for international use than growth
references developed in other countries. The NCHS references are poorly
modelled, and there is need for the data to be reanalysed in a more
sophisticated manner if they are to be of use internationally. In
cross-sectional studies, the use of Z scores as cut-offs for screening is to be
encouraged, since the lower centiles of NCHS are inaccurate. In longitudinal
use, workers should be aware that the tracking principle is flouted even by
healthy children in Western societies. Normal growth can better be described as
oscillation about a centile, rather that tracking along it. Thus short-term
deviation from a centile cannot be taken as evidence for pathology of any kind.

An international growth reference could be used for European and
European origin populations, as well as African, African origin and
Indo-Mediterranean populations. Current evidence suggests that they may not
apply to Asiatic populations, but in the absence of definitive evidence of a
cessation of the secular trend in any well-off Asiatic population, this
assumption must remain tentative. It is not clear whether genetically isolated
populations in various parts of the world including Africa, India, Latin America
and Asia are likely to show the same potential for growth when placed in
favourable environments. In addition, almost nothing is known about the genetic
potential for growth of Aboriginal populations in Australia, or in Pacific
Islands
populations.